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Abundances, diversity and seasonality of (non-extremophilic) Archaea in Alpine freshwaters

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Abstract

The objectives of this study were to assess abundances and community compositions of Archaea within a heterogeneous set of freshwater systems in the Austrian Alps. Seasonal changes and geographical differences within Archaea, considering abiotic and biotic factors (e.g. temperature, pH, total organic carbon (TOC), NH4 +, bacteria, fungi), were analysed in this context. Water samples were collected from 8 lakes, 10 creeks and the river Inn in 2014. Qualitative-quantitative data were derived via a comprehensive set of (quantitative) PCR assays and PCR-DGGE (denaturing gradient gel electrophoresis) based methodology, which was evaluated concerning specificity and reliability either previously or in this study. QPCR-derived archaeal abundances reached values of 103 copies mL−1 on average, with a peak in winter-spring (‘Cold Peak’), and covered 0–15 % (average: 1 %) of the microbial populations. This peak correlated with significantly raised TOC and low NH4 + levels during the cold seasons. Stagnant waters showed significantly higher archaeal abundances and diversities than flowing ones. Among methanogens, Methanosarcinales were the most common order. PCR-DGGE data showed that the archaeal communities were site-specific and could function as an ecological marker, in contrast to the more heterogeneous and unsteady bacterial and fungal community. This is attributable to the highly heterogeneous community of methanogenic Archaea (MA, Euryarchaeota), while only two species, Nitrosopumilus maritimus and Ca. Nitrososphaera gargensis, were found to be the ubiquitous representatives of ammonia-oxidizing Archaea (AOA, Thaumarchaeota) in Alpine freshwaters. This work emphasises the diversity, distribution and seasonality of non-extremophilic Archaea in Alpine freshwaters, with a first insight into their ecophysiological potential.

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References

  • Aller JY, Kemp PF (2008) Are archaea inherently less diverse than bacteria in the same environments? FEMS Microbiol Ecol 65:74–87

    Article  CAS  PubMed  Google Scholar 

  • Auguet JC, Casamayor EO (2008) A hotspot for cold crenarchaeota in the neuston of high mountain lakes. Environ Microbiol 10:1080–1086

    Article  CAS  PubMed  Google Scholar 

  • Auguet JC, Casamayor EO (2013) Partitioning of Thaumarchaeota populations along environmental gradients in high mountain lakes. FEMS Microbiol Ecol 84:154–164

    Article  CAS  PubMed  Google Scholar 

  • Auguet JC, Nomokonova N, Camarero L, Casamayor EO (2011) Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophicalpine lakes. Appl Environ Microbiol 6:1937–1945

    Article  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Battin TJ, Wille A, Sattler B, Psenner R (2001) Phylogenetic and functional heterogeneity of sediment biofilms along environmental gradients in a glacial stream. Appl Environ Microbiol 67:799–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruggen JJA, Zwart KB, Hermans JGF, Hove EM, Stumm CK, Vogels GD (1986) Isolation and characterization of Methanoplanus endosymbiosus sp. nov., an endosymbiont of the marine sapropelic ciliate Metopus contortus Quennerstedt. Arch Microbiol 144:367–374

    Article  Google Scholar 

  • Cao H, Auguet JC, Gu JD (2013) Global ecological pattern of ammonia-oxidizing Archaea. PLoS One 8:1–8

    CAS  Google Scholar 

  • Casamyor EO, Muyzer G, Pedros-Alio C (2001) Composition and temporal dynamics of planktonic archaeal assemblages from anaerobic sulfurous environments studied by 16S rDNA dneturing gradient gel electrophoresis and sequencing. Aquat Microb Ecol 25:237–246

    Article  Google Scholar 

  • Engel AS, Paoletti MG, Beggio M et al (2013) Comparative microbial community composition from secondary carbonate (moonmilk) deposits: implications for the Cansiliella servadeii cave hygropetric food web. Int J Speleol 42:181–192

    Article  Google Scholar 

  • Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive earth’s biogeochemical cycles. Science 320:1034–1039

    Article  CAS  PubMed  Google Scholar 

  • French E, Kozlowski JA, Mukherjee M, Bullerjahnb G, Bollmanna A (2012) Ecophysiological characterization of ammonia-oxidzing Archaea and bacteria from freshwater. Appl Environ Microbiol 78:5773–5780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fröhlich-Nowoisky J, Ruzene Nespoli C, Pickersgill DA, Galand PE, Müller-Germann I, Nunes T, Gomes Cardoso J, Almeida SM, Pio C, Andreae MO, Conrad R, Pöschl U, Després VR (2014) Diversity and seasonal dynamics of airborne Archaea. Biogeosciences 11:6067–6079

    Article  Google Scholar 

  • Galand PE, Lovejoy C, Vincent WF (2006) Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat Microb Ecol 44:115–126

    Article  Google Scholar 

  • Grossart HP, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. PNAS 108:19657–19661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez MH, Galand PE, Moffat C, Pantoja S (2015) Melting glacier impacts community structure of Bacteria. Environ Microbiol, Archaea and Fungi in a Chilean Patagonia fjord. doi:10.1111/1462-2920.12872

    Google Scholar 

  • Herfort L, Kim JH, Coolen MJL, Abbas B, Schouten S, Herndl GJ, Sinninghe Damste JS (2009) Diversity of Archaea and detection of crenarchaeotal amoA genes in the rivers Rhine and Têt. Aquat Microb Ecol 55:189–201

    Article  Google Scholar 

  • Hofmann K, Reitschuler C, Illmer P (2013) Aerobic and anaerobic microbial activities in the foreland of a receding glacier. Soil Biol Biochem 57:418–426

    Article  CAS  Google Scholar 

  • Hugoni M, Etien S, Bourges A, Lepèrea C, Domaizonc I, Malleta C, Bronnera G, Debroasa D, Marya I (2013) Dynamics of ammonia-oxidizing Archaea and bacteria in contrasted freshwater ecosystems. Res Microbiol 164:360–370

    Article  CAS  PubMed  Google Scholar 

  • Illmer P, Reitschuler C, Wagner AO, Schwarzenauer T, Lins P (2014) Microbial succession during thermophilic digestion: the potential of Methanosarcina sp. PLoS One. doi:10.1371/journal.pone.0086967

    PubMed  PubMed Central  Google Scholar 

  • Jurgens G, Glöckner FO, Amann R, Saano A, Montonen L, Likolammi M, Münster U (2000) Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization. FEMS Microbiol Ecol 34:45–56

    CAS  PubMed  Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils 6:68–72

    Article  CAS  Google Scholar 

  • Karner M, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510

    Article  CAS  PubMed  Google Scholar 

  • Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  CAS  PubMed  Google Scholar 

  • Lins P, Reitschuler C, Illmer P (2014) Methanosarcina spp., the key to relieve the start-up of a thermophilic anaerobic digestion suffering from high acetic acid loads. Biores Technol 152:347–354

    Article  CAS  Google Scholar 

  • Lipp JS, Morono Y, Inagaki F, Hinrichs KU (2008) Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454:991–994

    Article  CAS  PubMed  Google Scholar 

  • Manerkar MA, Seena S, Bärlocher F (2008) Q-RT-PCR for assessing archaea, bacteria, and fungi during leaf decomposition in a stream. Microb Ecol 56:467–473

    Article  CAS  PubMed  Google Scholar 

  • Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73:127–141

    Article  CAS  PubMed  Google Scholar 

  • Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Offre P, Spang A, Schleper C (2013) Archaea in biogeochemical cycles. Annu Rev Microbiol 67:437–457

    Article  CAS  PubMed  Google Scholar 

  • Pereyra LP, Hiibel SR, Prieto Riquelme MV, Reardon KF, Pruden A (2010) Detection and quantification of functional genes of cellulose-degrading, fermentative, and sulfate-reducing bacteria and methanogenic Archaea. Appl Environ Microbiol 76:2192–2202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pernthaler J, Glöckner FO, Unterholzner S, Alfreider A, Psenner R, Amann R (1998) Seasonal community and population dynamics of pelagic bacteria and Archaea in a high mountain lake. Appl Environ Microbiol 64:4299–4306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reche I, Pulido-Villena E, Morales-Baquero R, Casamyor EO (2005) Does ecosystem size determine aquatic bacterial richness? Ecology 86:1715–1722

    Article  Google Scholar 

  • Reitschuler C, Lins P, Illmer P (2014a) Primer evaluation and adaption for cost-efficient SYBR green-based qPCR and its applicability for specific quantification of methanogens. World J Microbiol Biotechnol 30:293–304

    Article  CAS  PubMed  Google Scholar 

  • Reitschuler C, Lins P, Wagner AO, Illmer P (2014b) Cultivation of moonmilk-born non-extremophilic Thaum and Euryarchaeota in mixed culture. Anaerobe 29:73–79

    Article  CAS  PubMed  Google Scholar 

  • Reitschuler C, Lins P, Schwarzenauer T, Spötl C, Wagner AO, Illmer P (2015) New undescribed lineages of non-extremophilic Archaea form a homogeneous and dominant element within alpine moonmilk microbiomes. Geomicrobiol J 32:890–902

    Article  CAS  Google Scholar 

  • Rooney-Varga JN, Anderson RT, Fraga JL, Ringelberg D, Lovley DR (1999) Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl Environ Microbiol 65:3056–3063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schabereiter-Gurtner C, Maca S, Rölleke S, Nigl K, Lukas J, Hirschl A (2001) 16S rDNA-based identification of bacteria from conjunctival swabs by PCR and DGGE fingerprinting. IOVS 42:1164–1171

    CAS  Google Scholar 

  • Silveira CB, Cardoso AM, Coutinho FH, Lima JL, Pinto LH, Albano RM, Clementino MM, Martins OB, Vieira RP (2013) Tropical aquatic Archaea show environment-specific community composition. PLoS One 8:11

    Google Scholar 

  • Tang KW, McGinnis DF, Frindte K, Brüchert V, Grossart HP (2014) Paradox reconsidered: methane oversaturation in well-oxygenated lake waters. Limnol Oceanogr 59:275–284

    Article  Google Scholar 

  • Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104:927–936

    Article  CAS  Google Scholar 

  • Vila-Costa M, Barberan A, Auguet JC, Sharma S, Moran MA, Casamayor EO (2013) Bacterial and archaeal community structure in the surface microlayer of high mountain lakes examined under two atmospheric aerosol loading scenarios. FEMS Microbiol Ecol 84:387–397

    Article  CAS  PubMed  Google Scholar 

  • Vissers EW, Blaga CI, Bodelier PLE, Muyzer G, Schleper C, Sinninghe Damste JS, Tourna M, Laanbroek HJ (2013) Seasonal and vertical distribution of putative ammonia-oxidizing thaumarchaeotal communities in an oligotrophic lake. FEMS Microbiol Ecol 83:515–526

    Article  CAS  PubMed  Google Scholar 

  • Wagner AO, Praeg N, Reitschuler C, Illmer P (2015) Effect of DNA extraction procedure, repeated extraction and ethidium monoazide (EMA)/propidium monoazide (PMA) treatment on overall DNA yield and impact on microbial fingerprints for bacteria, fungi and Archaea in a reference soil. Appl Soil Ecol 93:56–64

    Article  PubMed  PubMed Central  Google Scholar 

  • Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S, Sinninghe Damste JS (2006) Archaeal nitrification in the ocean. PNAS 104:12317–12322

    Article  Google Scholar 

  • Yu Y, Lee C, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    Article  CAS  PubMed  Google Scholar 

  • Zhang LM, Wang M, Prosser JI, Zheng YM, He JZ (2009) Altitude ammonia-oxidizing bacteria and Archaea in soils of Mount Everest. FEMS Microbiol Ecol 70:208–217

    Article  CAS  Google Scholar 

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Acknowledgments

We greatly thank Roswitha and Dieter Reitschuler as well as Stephanie Kistl for their logistical support and help during sampling.

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  1. Institute of Microbiology, University of Innsbruck, Technikerstrasse 25, 6020, Innsbruck, Austria

    Christoph Reitschuler, Katrin Hofmann & Paul Illmer

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  1. Christoph Reitschuler
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Correspondence to Christoph Reitschuler.

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Reitschuler, C., Hofmann, K. & Illmer, P. Abundances, diversity and seasonality of (non-extremophilic) Archaea in Alpine freshwaters. Antonie van Leeuwenhoek 109, 855–868 (2016). https://doi.org/10.1007/s10482-016-0685-6

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